Termination of translation: Interplay of mRNA, rRNAs and release factors?

EMBO Journal

Volumn 22, Issue 2, 2003, Pages 175-182

  Kisselev, Lev ^a   Ehrenberg, Måns ^b   Frolova, Ludmila ^a  

^a ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Polypeptide release factors; Ribosomes; RNA protein recognition; Translation

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; POLYPEPTIDE RELEASE FACTOR; PROTEIN; RIBOSOME RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ERF1; UNCLASSIFIED DRUG;

CODON; CONSENSUS SEQUENCE; ENZYME ACTIVITY; EUKARYOTE; OPEN READING FRAME; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA SEQUENCE; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; STOP CODON; TRANSLATION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CODON, TERMINATOR; GTP PHOSPHOHYDROLASES; HUMANS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE TERMINATION FACTORS; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; RNA, MESSENGER; RNA, RIBOSOMAL;

EUKARYOTA; PROKARYOTA;

EID: 0037439231     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg017     Document Type: Review

References (73)

1. Arkov,A.L. and Murgola,J. (1999) Ribosomal RNAs in translation termination: facts and hypotheses. Biochimiya (Moscow), 64, 1354-1359.
2. Bertram,G., Bell,H.A., Ritchie,D.W., Fullerton,G. and Stansfield,I. (2000) Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA, 6, 1236-1247.
3. Bertram,G., Innes,S., Minella,O., Richardson,J. and Stansfield,I. Endless possibilities: translation termination and stop codon recognition. Microbiology, 147, 255-269.
4. Buckingham,R.H., Grentzmann,G. and Kisselev,L. (1997) Polypeptide chain release factors. Mol. Microbiol., 24, 449-456.
5. Bulygin,K.N., Repkova,M.N., Ven'yaminova,A.G., Graifer,D.M., Karpova,G.G., Frolova,L.Yu. and Kisselev,L.L. (2002) Positioning of the mRNA stop signal with respect to polypeptide chain release factors and ribosomal proteins in 80S ribosomes. FEBS Lett., 514, 96-101.
6. Caskey,C.T. (1980) Peptide chain termination. Trends Biochem. Sci., 5, 234-237.
7. Chavatte,L., Frolova,L., Kisselev,L. and Favre,A. (2001) The polypeptide chain release factor eRF1 specifically contacts the s(4)UGA stop codon located in the A site of eukaryotic ribosomes. Eur. J. Biochem., 268, 2896-2904.
8. Chavatte,L., Seit-Nebi,A., Dubovaya,V. and Favre,A. (2002) The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J., 21, 5302-5311.
9. Cosson,B., Couturier,A., Chabelskaya,S., Kiktev,D., Inge-Vechtomov,S., Philippe,M. and Zhouravleva,G. (2002) Poly(A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI+] propagation. Mol. Cell Biol., 22, 3301-3315.
10. Czaplinski,K., Majlesi,N., Banerjee,T. and Peltz,S.W. (2000) Mttl is a Upfl-like helicase that interacts with the translation termination factors and whose overexpression can modulate termination efficiency. RNA, 6, 730-743.
11. Demeshkina,N., Repkova,V., Ven'yaminova,A., Graifer,D. and Karpova,G. (2000) Nucleotides of 18S rRNA surrounding mRNA codons at the human ribosomal A, P and E sites: a crosslinking study with mRNA analogs carrying an aryl azide group at either the uracil or the guanine residue. RNA, 6, 1727-1736.
12. Dinçbas-Renqvist,V., Engström,Å. Mora,L., Heurgué-Hamard,V., Buckingham,R.H. and Ehrenberg,M. (2000) A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J., 19, 6900-6907.
13. Dontsova,M., Frolova,L., Vassilieva,J., Piendl,W., Kisselev,L. and Garber,M. (2000) Translation termination factor aRF1 from the archaeon Methanococcus jannaschii is active with eukaryotic ribosomes. FEBS Lett., 472, 213-216.
14. Freistroffer,D.V., Pavlov,M.Y., MacDougall,J., Buckingham,R.H. and Ehrenberg,M. (1997) Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. EMBO J., 16, 4126-4133.
15. Freistroffer,D.V., Kwiatkowski,M., Buckingham,R.H. and Ehrenberg,M. (2000) The accuracy of codon recognition by polypeptide release factors. Proc. Natl Acad. Sci. USA, 97, 2046-2051.
16. Frolova,L. et al. (1994) A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature, 372, 701-703.
17. Frolova,L., Le Goff,X., Zhouravleva,G., Davydova,E., Philippe,M. and Kisselev,L. (1996) Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA, 2, 334-341.
18. Frolova,L.Y., Tsivkovskii,R.Y., Sivolobova,G.F., Oparina,N.Y., Serpinsky, O.I., Blinov,V.M., Tatkov,S.I. and Kisselev,L.L. (1999) Mutations in the highly conserved GGQ motif of class-1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA, 5, 1014-1020.
19. Frolova,L.Y., Merkulova,T.I. and Kisselev,L.L. (2000) Translation termination in eukaryotes: polypeptide release factor eRF1 is composed of functionally and structurally distinct domains. RNA, 6, 381-390.
20. Frolova,L., Seit-Nebi,A. and Kisselev,L. (2002) Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA, 8, 129-136.
21. Green,R. and Noller,H.F. (1997) Ribosomes and translation. Annu. Rev. Biochem., 66, 679-716.
22. Grentzmann,G., Brechemier-Baey,D., Heurgué,V., Mora,L. and Buckingham,R.H. (1994) Localization and characterization of the gene encoding release factor RF3 in Escherichia coli. Proc. Natl Acad. Sci. USA, 91, 5848-5852.
23. Grentzmann,G., Kelly,P.J., Laalami,S., Shuda,M., Firpo,M.A., Cenatiempo,Y. and Kaji,A. (1998) Release factor RF-3 GTPase activity acts in disassembly of the ribosome termination complex. RNA, 8, 973-983.
24. Heurgué-Hamard,V., Karimi,R., Mora,L., MacDougall,J., Leboeuf,C., Grentzmann,G., Ehrenberg,M. and Buckingham,R.H. (1998) Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome. EMBO J., 17, 808-816.
25. Hoshino,S., Imai,M., Mizutani,M., Kikuchi,Y., Hanaoka,F., Ui,M. and Katada,T. (1998) Molecular cloning of a novel member of the eukaryotic polypeptide chain-releasing factors (eRF). Its identification as eRF3 interacting with eRF1. J. Biol. Chem., 273, 22254-22259.
26. Hoshino,S., Imai,M., Kobayashi,T., Uchida,N. and Katada,T. (1999) The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-poly(A) tail of mRNA. Direct association of eRF3/GSPT with polyadenylate-binding protein. J. Biol. Chem., 274, 16677-16680.
27. Inagaki,Y. and Doolittle,W.F. (2001) Class I release factors in ciliates with variant genetic codes. Nucleic Acids Res., 29, 921-927.
28. Inagaki,Y., Blouin,C., Doolittle,W.F. and Roger,A.J. (2002) Convergence and constraint in eukaryotic release factor (eRF1) domain 1: the evolution of stop codon specificity. Nucleic Acids Res., 30, 532-544.
29. Ito,K., Uno,M. and Nakamura,Y. (2000) A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature, 403, 680-684.
30. Ito,K., Frolova,L., Seit-Nebi,A., Karamyshev,A., Kisselev,L. and Nakamura,Y. (2002) Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within the domain 1. Proc. Natl Acad. Sci. USA, 99, 8494-8499.
31. Ivanov,V., Beniaminov,A., Mikheev,A. and Minyat,E. (2001) A mechanism for stop codon recognition by the ribosome: a bioinformatic approach. RNA, 7, 1683-1692.
32. Jacobsen,C.G., Segaard,T.M.M., Jean-Jean,O., Frolova,L. and Justesen,J. (2001) Identification of eRF3b, a human polypeptide chain release factor with eRF3 activity in vitro and in vivo. Mol. Biol., 35, 672-681.
33. Janosi,L., Hara,H., Zhang,S. and Kaji,A. (1996) Ribosome recycling by ribosome recycling factor (RRF) - an important but overlooked step of protein biosynthesis. Adv. Biophys., 32, 121-201.
34. Janzen,D.M. and Geballe,A.P. (2001) Modulation of translation termination mechanisms by cis- and trans-acting factors. Cold Spring Harbor Symp. Quant. Biol., 66, 459-467.
35. Janzen,D.M., Frolova,L. and Geballe,A. (2002) Inhibition of translation termination mediated by an interaction of eukaryotic release factor 1 with a nascent peptidyl-tRNA. Mol. Cell. Biol., 22, 8562-8570.
36. Karimi,R., Pavlov,M.Y., Buckingham,R.H. and Ehrenberg,M. (1999) Novel roles for classical factors at the interface between translation termination and initiation. Mol. Cell, 3, 601-609.
37. Kervestin,S., Frolova,L., Kisselev,L. and Jean-Jean,O. (2001) Stop codon recognition in ciliates: Euplotes release factor does not respond to reassigned UGA codon. EMBO Rep., 2, 680-684.
38. Kisselev,L.L. and Buckingham,R.H. (2000) Translation termination comes of age. Trends Biochem. Sci., 25, 561-566.
39. Kisselev,L.L., Oparina,N.Yu. and Frolova,L.Yu. (2000) Class-1 polypeptide chain release factors are structurally and functionally similar to suppressor tRNAs and comprise different structural-functional families of prokaryotic/mitochondrial and eukaryotic/archaebacterial factors. Mol. Biol., 34, 427-442.
40. Knight,R.D., Freeland,S.J. and Landweber,L.F. (2001) Rewiring the keyboard: evolvability of the genetic code. Nat. Rev. Genet., 2, 49-58.
41. Kushnirov,V.V., Ter-Avanesyan,M.D., Telckov,M.V., Surguchov,A.P., Smirnov,V.N. and Inge-Vechtomov,S.G. (1988) Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene, 66, 45-54.
42. Liang,A., Brunen-Nieweler,C., Muramatsu,T., Kuchino,Y., Beier,H. and Heckmann,K. (2001) The ciliate Euplotes octocarinatus expresses two polypeptide release factors of the type eRF1. Gene, 262, 161-168.
43. Lozupone,C.A., Knight,R.D. and Landweber,L.F. (2001) The molecular basis of nuclear genetic code change in ciliates. Curr. Biol., 11, 65-74.
44. Merkulova,T.I., Frolova,L.Y., Lazar,M., Camonis,J. and Kisselev,L.L. (1999) C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett., 443, 41-47.
45. Mikuni,O., Ito,K., Moffat,J., Matsumura,K., McCaughan,K., Nobukuni,T., Tate,W. and Nakamura,Y. (1994) Identification of the prfC gene, which encodes peptide chain release factor 3 of Escherichia coll. Proc. Natl Acad. Sci. USA, 91, 5798-5802.
46. Moazed,D. and Noller,H.F. (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature, 327, 389-394.
47. Moffat,J.G. and Tate,W.P. (1994) A single proteolytic cleavage in release factor 2 stabilizes ribosome binding and abolishes peptidyl-tRNA hydrolysis activity. J. Biol. Chem., 269, 18899-18903.
48. Mora,L., Heurgué-Hamard,V., Champ,S., Ehrenberg,M., Kisselev,L.L. and Buckingham,R.H. (2003) The essential role of the invariant GGQ motif in the function and the stability in vivo of bacterial release factors RF1 and RF2. Mol. Microbiol., in press.
49. Mortensen,K.K., Hansen,H.F., Grentzmann,G., Buckingham,R.H. and Sperling-Petersen,H.U. (1995) Osmo-expression and fast two-step purification of Escherichia coli translation termination factor RF-3. Eur. J. Biochem., 34, 732-736.
50. Nakamura,Y. and Ito,K. (1998) How protein reads the stop codon and terminates translation. Genes Cells, 3, 265-278.
51. Nakamura,Y. and Ito,K. (2002) A tripeptide discriminator for stop codon recognition. FEBS Lett., 514, 30-33.
52. Nakamura,Y., Ito,K. and Isaksson,L.A. (1996) Emerging understanding of translation termination. Cell, 87, 147-150.
53. Nakamura,Y., Ito,K. and Ehrenberg,M. (2000) Mimicry grasps reality in translation termination. Cell, 101, 349-352.
54. Paulin,E.M., Campbell,L.E., O'Brien,K., Loughlin,J. and Proud,C.G. (2001) Eukaryotic translation initiation factor 5 (elF5) acts as a classical GTPase-activator protein. Curr. Biol., 11, 55-59.
55. Pel,H.J., Moffat,J.G., Ito,K., Nakamura,Y. and Tate,W.P. (1998) Escherichia coli release factor 3: resolving the paradox of a typical G protein structure and atypical function with guanine nucleotides. RNA, 4, 47-54.
56. Poole,E. and Tate,W. (2000) Release factors and their role as decoding proteins: specificity and fidelity for termination of protein synthesis. Biochim. Biophys. Acta, 1493, 1-11.
57. Ramakrishnan,V. (2002) Ribosome structure and the mechanism of translation. Cell, 108, 557-572.
58. Ruusala,T., Ehrenberg,M., Caskey,C.T. and Nirenberg,M. (1982) Is there proof-reading during polypeptide synthesis? EMBO J., 1, 741-745.
59. Seit-Nebi,A., Frolova,L., Ivanova,N., Poltaraus,A. and Kisselev,L. (2000) Substitutions of the glutamine residue in ubiquitous GGQ tripeptide in human eRF1 do not entirely abolish the release factor activity. Mol. Biol. (Mosk.), 34, 899-900.
60. Seit-Nebi,A., Frolova,L., Justesen,J. and Kisselev,L. (2001) Class-1 translation termination factors: invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition. Nucleic Acids Res., 29, 3982-3987.
61. Seit-Nebi,A., Frolova,L. and Kisselev,L. (2002) Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep., 9, 881-886.
62. Scheffzek,K., Ahmadian,M.R. and Wittinghofer,A. (1998) GTPase-activating proteins: helping hands to complement an active site. Trends Biochem. Sci., 23, 257-262.
63. Song,H., Mugnier,P., Das,A.K., Webb,H.M., Evans,D.R., Tuite,M.F., Hemmings,B.A. and Barford,D. (2000) The crystal structure of human eukaryotic release factor eRF1 - mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell, 100, 311-321.
64. Szkaradkiewicz,K., Nanninga,M., Nesper-Brock,M., Gerrits,M., Erdmann,V.A. and Sprinzl,M. (2002) RNA aptamers directed against release factor 1 from Thermus thermophilus. FEBS Lett., 514, 90-95.
65. Urakov,V.N., Valouev,I.A., Lewitin,E.I., Paushkin,S.V., Kosorukov, V.S., Kushnirov,V.V., Smirnov,V.N. and Ter-Avanesyan,M.D. (2001) IttIp, a novel protein inhibiting translation termination in Saccharomyces cerevisiae. BMC Mol. Biol., 2, 9.
66. Velichutina,I.V., Hong,J.Y., Mesecar,A.D., Chernoff,Y.O. and Liebman, S.W. (2001) Genetic interaction between yeast Saccharomyces cerevisiae release factors and the decoding region of 18S rRNA. J. Mol. Biol., 305, 715-727.
67. Vestergaard,B., Van,L.B., Andersen,G.R., Nyborg,J., Buckingham,R.H. and Kjeldgaard,M. (2001) Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell, 8, 1375-1382.
68. Wang,W., Czaplinski,K., Rao,Y. and Peltz,W. (2001) The role of Upf proteins in modulating the translation read-trough of nonsense-containing transcripts. EMBO J., 20, 880-890.
69. Wilson,D.N., Blaha,G., Connell,S.R., Ivanov,P.V., Jenke,H., Stelzl,U., Teraoka,Y. and Nierhaus,K.H. (2002) Protein synthesis at atomic resolution: mechanistics of translation in the light of highly resolved structures for the ribosome. Curr. Protein Peptide Sci., 3, 1-53.
70. Wilson,P.G. and Culbertson,M.R. (1988) SUF12 suppressor protein of yeast. A fusion protein related to the EF-1 family of elongation factors. J. Mol. Biol., 199, 559-573.
71. Zavialov,A.V., Buckingham,R.H. and Ehrenberg,M. (2001) A post-termination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell, 107, 115-124.
72. Zavialov,A.V., Mora,L., Buckingham,R.H. and Ehrenberg,M. (2002) Release of peptide promoted by the GGQ-motif of class-1 release factors regulates the GTPase activity of RF3. Mol. Cell, 10, 789-798.
73. Zhouravleva,G., Frolova,L., Le Goff,X., Le Guellec,R., Inge-Vechtomov,S., Kisselev,L. and Philippe,M. (1995) Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J., 14, 4065-4072.